Broad-scale reciprocity in an avian seed dispersal mutualism

Aim Coevolved relationships between individual species of birds and plants rarely occur in seed dispersal mutualisms. This study evaluates whether reciprocal relationships may occur between assemblages of bird and plant species. Location Vancouver Island, British Columbia, Canada (48°50′‐N, 125°22′‐W). Methods The distribution and fruiting phenologies of seven shrub species were compared to seasonal changes in habitat selection and seed dispersal by six fruit‐eating bird species. Results Shrub species inhabiting forest understorey habitat had earlier fruiting phenologies than shrub species inhabiting forest edge habitat along lake and bog margins. Birds showed a parallel pattern in habitat selection, being more abundant in the forest understorey early in the fruiting season, and more abundant in the forest edge later in the season. Rates of seed deposition covaried with avian habitat selection, in such a way that birds directed seed dispersal into habitats preferred by shrubs. Conclusions These results depict a broad‐scale pattern in the abundance of birds and fruits indicative of reciprocal interactions. Seasonal changes in seed dispersal to each habitat appear to reinforce the relationship between shrub habitat affinities and fruiting phenologies. Phenological differences between habitats may also reinforce seasonal changes in avian habitat selection. Therefore, although reciprocal interactions between pairs of bird and plant species are rare, broad‐scale reciprocal relationships may occur between assemblages of bird and plant species.     

Contagious dispersal of seeds of synchronously fruiting species beneath invasive and native fleshy‐fruited trees

In subtropical Australia, many native and invasive plant species rely on a shared suite of frugivores, largely birds, for seed dispersal. Many native plants fruit during summer in this region, whereas most invasive plants fruit during winter, thus providing the opportunity for contagious dispersal of seeds beneath synchronously fruiting species. We sampled invasive and native seed rain beneath the canopy of a native summer‐fruiting tree Guioa semiglauca and an invasive winter‐fruiting tree Cinnamomum camphora, in three study sites over the course of a year. In July, during peak fruiting season for C. camphora and other invasive species, seed rain of invasive species was higher beneath C. camphora than G. semiglauca. This was partly due to the invasive tree Ligustrum lucidum, whose seed rain was three times higher beneath C. camphora than beneath the native tree. In February, seed rain of native species was more abundant beneath the canopy of G. semiglauca than beneath C. camphora, despite the fact that C. camphora was also fruiting at this time. This was probably due to the larger fruit crop produced by G. semiglauca at this time of year. Our study provides evidence that the presence of invasive bird‐dispersed plants may facilitate contagious seed dispersal of other invaders, and likewise native species may facilitate seed spread of other native plants.     

Seed Dispersal Modes of the Sandstone Plateau Vegetation of the Middle Caquetá River Region,Colombian Amazonia1

We characterized the dispersal spectra and phenology of 298 vascular plant species of the sandstone plateaus of Colombian Amazonia. Dispersal modes were determined by the morphology of dispersion units, personal observations on fruit consumption, and an extensive literature review. We obtained the number of species per dispersal mode for the sandstone plateaus and for two recognized vegetation types: open‐herbaceous vegetation and low forest‐shrub vegetation. Dispersal modes were assigned to 295 plant species. Animals dispersed the highest percentage of species (46.6%), while the percentage of autochorous and anemochorous species was 29.4 and 23 percent, respectively. The dispersal spectrum of the low forest‐shrub vegetation type, based on the coverage of every species, showed that percentages of anemochorous (40.2%) and zoochorous species (37.8%) were similar. Autochory was the most important seed dispersal mode of the open‐herbaceous vegetation (60%). Birds were the principal group of potential dispersers (58.9%) of zoochorous species and reptiles the least important. We found two marked fruiting peaks, one from the end of the dry season to the beginning of the wet season and the second one from the beginning to the middle of the dry season. Our results showed that besides the differences in the vegetation structure and floristic composition between the sandstone plateaus and the adjacent tall forest, there also exist differences in the dispersal spectra and the fruiting rhythms.     

Seed dispersal by animals: exact identification of source trees with endocarp DNA microsatellites

A long-standing challenge in studies of seed dispersal by animal frugivores has been the characterization of the spatial relationships between dispersed seeds and the maternal plants, i.e. the seed shadow. The difficulties to track unambiguously the origin of frugivore-dispersed seeds in natural communities has been considered an unavoidable limitation of the research field and precluded a robust analysis of the direct consequences of zoochory. Here we report that the multilocus genotype at simple sequence repeat (SSR; microsatellite) loci of the woody endocarp, a tissue of maternal origin, provides an unequivocal genetic fingerprint of the source tree. By comparing the endocarp genotype against the complete set of genotypes of reproductive trees in the population, we could unambiguously identify the source tree for 82.1% of the seeds collected in seed traps and hypothesize that the remaining 17.9% of sampled seeds come from other populations. Identification of the source tree for Prunus mahaleb seeds dispersed by frugivores revealed a marked heterogeneity in the genetic composition of the seed rain in different microhabitats, with a range of 1-5 distinct maternal trees contributing seeds to a particular landscape patch. Within-population dispersal distances ranged between 0 and 316 m, with up to 62% of the seeds delivered within 15 m of the source trees. Long distance dispersal events, detected by the exclusion of all reproductive trees in the population, accounted for up to 17.9% of the seeds sampled. Our results indicate strong distance limitation of seed delivery combined with infrequent long-distance dispersal events, extreme heterogeneity in the landscape pattern of genetic makeup, and a marked mosaic of multiple parentage for the seeds delivered to a particular patch.     

Limited dispersal and geographic barriers cause population differentiation and structuring in Begonia maxwelliana at both large and small scales

Background: Genetic divergence is one of the key processes in speciation. In the Begoniaceae, genetic divergence caused by limited gene flow may explain its high species diversity and endemicity. This hypothesis has been supported by past genetic work but there is a lack of empirical studies on the causes of limited gene flow.

Aim: To identify the causes of limited gene flow in Begonia.

Methods: We examined the genetic structure among the populations of Begonia maxwelliana at the macro- and micro-spatial scales using microsatellites, measured seed dispersal range and observed flowering phenology.

Results: Population differentiation and structuring were detected at both the macro- and micro-scales. Dispersal range was short, and all populations showed similar reproductive behaviour.

Conclusions: The strong population differentiation and structuring among the populations studied imply that they are evolutionarily significant units and possible candidates for speciation. Geographical barriers and limited seed dispersal restrict gene flow in the populations, and these factors may be responsible for the rapid speciation and large diversity in the family.     

Negative correlation between altitudes and oxygen isotope ratios of seeds: exploring its applicability to assess vertical seed dispersal

Vertical seed dispersal, which plays a key role in plant escape and/or expansion under climate change, was recently evaluated for the first time using negative correlation between altitudes and oxygen isotope ratio of seeds. Although this method is innovative, its applicability to other plants is unknown. To explore the applicability of the method, we regressed altitudes on δ¹⁸O of seeds of five woody species constituting three families in temperate forests in central Japan. Because climatic factors, including temperature and precipitation that influence δ¹⁸O of plant materials, demonstrate intensive seasonal fluctuation in the temperate zone, we also evaluated the effect of fruiting season of each species on δ¹⁸O of seeds using generalized linear mixed models (GLMM). Negative correlation between altitudes and δ¹⁸O of seeds was found in four of five species tested. The slope of regression lines tended to be lower in late‐fruiting species. The GLMM analysis revealed that altitudes and date of fruiting peak negatively affected δ¹⁸O of seeds. These results indicate that the estimation of vertical seed dispersal using δ¹⁸O of seeds can be applicable for various species, not just confined to specific taxa, by identifying the altitudes of plants that produced seeds. The results also suggest that the regression line between altitudes and δ¹⁸O of seeds is rather species specific and that vertical seed dispersal in late‐fruiting species is estimated at a low resolution due to their small regression slopes. A future study on the identification of environmental factors and plant traits that cause a difference in δ¹⁸O of seeds, combined with an improvement of analysis, will lead to effective evaluation of vertical seed dispersal in various species and thereby promote our understanding about the mechanism and ecological functions of vertical seed dispersal.     

Long‐term consistency in spatial patterns of primate seed dispersal

Seed dispersal is a key ecological process in tropical forests, with effects on various levels ranging from plant reproductive success to the carbon storage potential of tropical rainforests. On a local and landscape scale, spatial patterns of seed dispersal create the template for the recruitment process and thus influence the population dynamics of plant species. The strength of this influence will depend on the long‐term consistency of spatial patterns of seed dispersal. We examined the long‐term consistency of spatial patterns of seed dispersal with spatially explicit data on seed dispersal by two neotropical primate species, Leontocebus nigrifrons and Saguinus mystax (Callitrichidae), collected during four independent studies between 1994 and 2013. Using distributions of dispersal probability over distances independent of plant species, cumulative dispersal distances, and kernel density estimates, we show that spatial patterns of seed dispersal are highly consistent over time. For a specific plant species, the legume Parkia panurensis, the convergence of cumulative distributions at a distance of 300 m, and the high probability of dispersal within 100 m from source trees coincide with the dimension of the spatial–genetic structure on the embryo/juvenile (300 m) and adult stage (100 m), respectively, of this plant species. Our results are the first demonstration of long‐term consistency of spatial patterns of seed dispersal created by tropical frugivores. Such consistency may translate into idiosyncratic patterns of regeneration.     

Seed traits matter—Endozoochoric dispersal through a pervasive mobile linker

Although many plants are dispersed by wind and seeds can travel long distances across unsuitable matrix areas, a large proportion relies on co‐evolved zoochorous seed dispersal to connect populations in isolated habitat islands. Particularly in agricultural landscapes, where remaining habitat patches are often very small and highly isolated, mobile linkers as zoochorous seed dispersers are critical for the population dynamics of numerous plant species. However, knowledge about the quali‐ or quantification of such mobile link processes, especially in agricultural landscapes, is still limited. In a controlled feeding experiment, we recorded the seed intake and germination success after complete digestion by the European brown hare (Lepus europaeus) and explored its mobile link potential as an endozoochoric seed disperser. Utilizing a suite of common, rare, and potentially invasive plant species, we disentangled the effects of seed morphological traits on germination success while controlling for phylogenetic relatedness. Further, we measured the landscape connectivity via hares in two contrasting agricultural landscapes (simple: few natural and semi‐natural structures, large fields; complex: high amount of natural and semi‐natural structures, small fields) using GPS‐based movement data. With 34,710 seeds of 44 plant species fed, one of 200 seeds (0.51%) with seedlings of 33 species germinated from feces. Germination after complete digestion was positively related to denser seeds with comparatively small surface area and a relatively slender and elongated shape, suggesting that, for hares, the most critical seed characteristics for successful endozoochorous seed dispersal minimize exposure of the seed to the stomach and the associated digestive system. Furthermore, we could show that a hare''s retention time is long enough to interconnect different habitats, especially grasslands and fields. Thus, besides other seed dispersal mechanisms, this most likely allows hares to act as effective mobile linkers contributing to ecosystem stability in times of agricultural intensification, not only in complex but also in simple landscapes.     

西双版纳地区鞘花的繁殖物候特征及影响因素

桑寄生植物作为关键种和关键性食物资源在生态系统中扮演着重要角色,其鞘花的繁殖物候特征不仅会影响自身的繁殖适合度而且还会影响依赖于其获取食物资源的动物。为了解鞘花的繁殖物候特征及其影响因素,探究其与寄主植物和种子散布者之间的相互作用关系。该研究以西双版纳地区分布的鞘花为对象,通过定期观测鞘花和其寄主植物木荷的繁殖物候,测量它们的生物学特性和温湿度等环境因子,并分析鞘花在个体水平和种群水平上的繁殖物候特征以及寄主植物和温湿度对其繁殖物候的影响。结果表明:(1)鞘花的开花物候属于集中大量开花模式,整个种群的花期和果期的持续时间分别约为20 d和72 d,花期和果期的同步性指数都较高,6月中旬鞘花果实被取食的数量和速率最大,之后逐渐降低。(2)鞘花的始花期与木荷的始花期相关性较高,花期和果期与木荷的繁殖物候基本重叠。(3)每月开花和果熟的个体数量与同期和前一个月的平均温度和相对湿度的相关关系均不显著。总之,桑寄生植物的繁殖物候特征可能受到较多因素的影响,若想全面了解半寄生植物的繁殖物候特征,就要综合考虑生物和非生物等多种因子的共同作用。     

Interactions between body size,abundance, seasonality,and phenology in forest beetles

Body size correlates with a large number of species traits, and these relationships have frequently been used to explain patterns in populations, communities, and ecosystems. However, diverging patterns occur, and there is a need for more data on different taxa at different scales. Using a large dataset of 155,418 individual beetles from 588 species collected over 13 years of sampling in Norway, we have explored whether body size predicts abundance, seasonality, and phenology in insects. Seasonality is estimated here by flight activity period length and phenology by peak activity. We develop several methods to estimate these traits from low‐resolution sampling data. The relationship between abundance and body size was significant and as expected; the smaller species were more abundant. However, smaller species tended to fly for longer periods of the summer and peaked in midsummer, while larger species were restricted to shorter temporal windows. Further analysis of repeated sampling from a single location suggested that smaller species had increased flight period lengths in warmer years, but larger species showed the opposite pattern. The results 1) indicate that smaller species are likely to be disproportionately valuable in ecological interactions, and 2) provide potential insights into the traits influencing the vulnerability of some larger species to disturbances and climate change.     

Seed Dispersal Spectrum of Woody Species in South Ecuadorian Dry Forests: Environmental Correlates and the Effect of Considering Species Abundance

This study examines the seed dispersal spectrum of the tropical dry forests of Southern Ecuador, in an effort to contribute to the knowledge of the complex dynamics of tropical dry forests. Seed dispersal spectrum was described for a total number of 160 species. Relationships of dispersal syndromes with plant growth form and climatic seasonality were explored. For a subset of 97 species, we determined whether dispersal spectrum changes when species abundance, in addition to species number, is taken into account. The same subset was used to relate dispersal syndromes with the environmental conditions. Zoochorous species dominated in the studied community. When considering the individual abundance of each species, however, anemochory was the prevalent dispersal syndrome. We found a significant difference in the frequency of dispersal syndromes among plant growth forms, with epizoochory only occurring in shrub species. The dispersal spectrum was dependent on climatic seasonality. The largest proportion of anemochorous species fructified during the dry season, while zoochorous diaspores dominated during the rainy season. A fourth‐corner analysis indicated that the seed dispersal spectrum of Southern Ecuador dry forests is controlled by environmental conditions such as annual precipitation, annual temperature range or topography. Our results suggest that spatio‐temporal changes in the environmental conditions may affect important ecological processes for dispersal. Thus, the predominance of one syndrome or another may depend on the spatial variation of environmental conditions. Abstract in Spanish is available at http://www.blackwell‐synergy.com/loi/btp .     

Scale and macroecological patterns in seed dispersal mutualisms

Although some studies of seed dispersal mutualisms have documented adaptive relationships between fruits and frugivores, others have shown that adaptive patterns are constrained by phylogenetic, historical or climatic effects. Variable results among studies have thwarted attempts to find a paradigm to unite the field and direct research. Two recent studies in Global Ecology and Biogeography exemplify this dichotomy. One paper reported adaptive relationships between abundances of birds and fruits, while the other study found that bird‐fruit abundance patterns were constrained by climatic effects. Almost paradoxically, both studies were conducted at the same locale. However, they focused on different spatio‐temporal scales. These results are surprisingly consistent with several other recent studies that have taken a macroecological approach. They also indicate that mutualistic relationships between fruits and frugivores are scale dependent. When viewed together, recent work suggests that the conflicting results of previous studies may result from spatio‐temporal variability of mutualistic relationships. This paper briefly reviews the emerging field of seed dispersal macroecology. A growing appreciation for scale appears to be leading the field in a new direction.     

Spatio–temporal Variations in Post‐dispersal Seed Fate1

The post‐dispersal fate of Chrysophyllum lucentifolium (a canopy tree; Sapotaceae) seeds was analyzed in French Guiana over three consecutive years. Experiments using 750 thread‐marked seeds were performed to investigate seed removal, predation, and caching by terrestrial vertebrates on howler monkey (Alouatta seniculus) defecation sites, where clumps of intact C. lucentifolium seeds were observed. Year‐to‐year variations in seed fate during the peak fruiting period were considered in relation to overall fruit and seed resource availability estimated by a raked‐trail survey. The effect of two forest areas, which differed in soil and floristic composition, was examined with conspecific fruiting tree density as a covariant. Exclosure versus open treatment was used to discriminate small rodents (not larger than a spiny rat) from other vertebrates. The presence of fresh howler dung did not affect seed fate after 20 days as shown by comparisons between defecation sites and control during the first year. There was a significant effect of year on the percentage of seeds remaining after 20 days. Low seed removal in 1995 and 1996 (compared to 1997) corresponded to higher overall fruiting and higher fruiting of C. lucentifolium, or the presence of alternative resources for rodents. An effect of forest area was observed on the seed removal rate, which varied with years and protection. Comparatively, an effect of forest area on the percentage of seeds lost was observed in 1996 and an effect of treatment on the percentage of seeds eaten was seen in 1995. The mode of seed caching suggested that spiny rats were the main seed remover. Results of this study suggest that greater seedling recruitment may occur when large fruit crop and high howler dispersal co‐occur with a lower impact of rodents (i.e., when rodents are saturated by abundant and diversified fruit resources such as in 1995). Such event synchrony, however, is highly unpredictable after only three years of study.     

Seed dispersal by ants in the semi-arid Caatinga of North-East Brazil

BACKGROUND AND AIMS: Myrmecochory is a conspicuous feature of several sclerophyll ecosystems around the world but it has received little attention in the semi-arid areas of South America. This study addresses the importance of seed dispersal by ants in a 2500-km(2) area of the Caatinga ecosystem (north-east Brazil) and investigates ant-derived benefits to the plant through myrmecochory. METHODS: Seed manipulation and dispersal by ants was investigated during a 3-year period in the Xingó region. Both plant and ant assemblages involved in seed dispersal were described and ant behaviour was characterized. True myrmecochorous seeds of seven Euphorbiaceae species (i.e. elaiosome-bearing seeds) were used in experiments designed to: (1) quantify the rates of seed cleaning/removal and the influence of both seed size and elaiosome presence on seed removal; (2) identify the fate of seeds dispersed by ants; and (3) document the benefits of seed dispersal by ants in terms of seed germination and seedling growth. KEY RESULTS: Seed dispersal by ants involved one-quarter of the woody flora inhabiting the Xingó region, but true myrmecochory was restricted to 12.8 % of the woody plant species. Myrmecochorous seeds manipulated by ants faced high levels of seed removal (38-84 %) and 83 % of removed seeds were discarded on ant nests. Moreover, seed removal positively correlated with the presence of elaiosome, and elaiosome removal increased germination success by at least 30 %. Finally, some Euphorbiaceae species presented both increased germination and seedling growth on ant-nest soils. CONCLUSIONS: Myrmecochory is a relevant seed dispersal mode in the Caatinga ecosystem, and is particularly frequent among Euphorbiaceae trees and shrubs. The fact that seeds reach micro-sites suitable for establishment (ant nests) supports the directed dispersal hypothesis as a possible force favouring myrmecochory in this ecosystem. Ecosystems with a high frequency of myrmecochorous plants appear not to be restricted to regions of nutrient-impoverished soil or to fire-prone regions.     

Contemporary pollen and seed dispersal in a Prunus mahaleb population: patterns in distance and direction

Pollination and seed dispersal determine the spatial pattern of gene flow in plant populations and, for those species relying on pollinators and frugivores as dispersal vectors, animal activity plays a key role in determining this spatial pattern. For these plant species, reported dispersal patterns are dominated by short-distance movements with a significant amount of immigration. However, the contribution of seed and pollen to the overall contemporary gene immigration is still poorly documented for most plant populations. In this study we investigated pollination and seed dispersal at two spatial scales in a local population of Prunus mahaleb (L.), a species pollinated by insects and dispersed by frugivorous vertebrates. First, we dissected the relative contribution of pollen and seed dispersal to gene immigration from other parts of the metapopulation. We found high levels of gene immigration (18.50%), due to frequent long distance seed dispersal events. Second, we assessed the distance and directionality for pollen and seed dispersal events within the local population. Pollen and seed movement patterns were non-random, with skewed distance distributions: pollen tended moved up to 548 m along an axis approaching the N-S direction, and seeds were dispersed up to 990 m, frequently along the SW and SE axes. Animal-mediated dispersal contributed significantly towards gene immigration into the local population and had a markedly nonrandom pattern within the local population. Our data suggest that animals can impose distinct spatial signatures in contemporary gene flow, with the potential to induce significant genetic structure at a local level.     

Seed dispersal and seedling recruitment of trees at different successional stages in a temperate forest in northeastern China

Aims Spatial distribution of adult trees in a forest community is determined by patterns of both seed dispersal and seedling recruitment. The objectives of our study were to understand the processes of seed dispersal and seedling recruitment of dominant tree species in a temperate forest of northeastern China and to identify the factors constraining seed dispersal and seedling establishment at different stages of forest succession.Methods During three summer and autumn sessions between 2006 and 2008, altogether 113080 seeds from 22 different tree species were collected in three large field plots representing different forest types in the Changbai Mountain region of northeastern China. The spatial distribution of seed abundance was analyzed using a Syrjala test. Regeneration success of nine major tree species was assessed using variables defining 'limitations' in 'seeds' and 'seedling establishment'.Important findings We found that seed production fluctuated between years and varied greatly with forest types. Four tree species, Acer spp., Fraxinus mandshurica, Tilia amurensis and Betula spp., had the greatest seed production and the widest range of seed dispersal, whereas Quercus mongolica showed the most sustained seed production pattern. The spatial patterns of seed abundance differed significantly among forest types and years. The tree species investigated in this study differed in the degree of seed limitation, as well as in limitation of seedling establishment. There were both negative and positive correlations between seed density and seedling density, depending on site and parental tree density. Seeds of 16 tree species were found in the Populus davidiana–Betula platyphylla forest (PBF) plot, 11 in the conifer and broad-leaved mixed forest (CBF) plot but only 8 in the broad-leaved-Korean pine mixed forest (BKF) plot. The number of seed-contributing species was not only greater in the secondary forests (CBF and PBF plots) than in the primary forest (BKF plot) but was also more variable during the 3 years of assessment. Results from the correlations between seed density and seedling occurrence and that between parental tree density or seed weight and dispersal limitation confirm our intuitive expectations, i.e. heavy seeds had greater dispersal limitation but higher establishment success than light seeds.